An emerging coastal wetland management dilemma between mangrove expansion and shorebird conservation

Abstract Coastal wetlands around the world have been degraded by human activities. Global declines in the extent of important coastal wetlands, including mangroves, salt marshes, and tidal flats, necessitate mitigation and restoration efforts. However, some well‐meaning management actions, particularly mangrove afforestation, can inadvertently cause further loss and degradation of other habitats if these actions are not planned carefully. In particular, there is a potential conflict between mangrove and shorebird conservation because mangrove afforestation and restoration may occur at the expense of bare tidal flats, which form the main foraging habitats for threatened shorebirds and support other coastal organisms. We examined several case studies that illustrate the trade‐off between mangrove restoration and bare tidal flat maintenance. To investigate whether these examples reflect an emerging broad‐scale problem, we used satellite imagery to quantify the change in mangrove habitat extent in 22 important shorebird areas in mainland China from 2000 to 2015.The extent of tidal flat across all sites declined significantly (p < 0.01, n = 22) while among sites with mangroves present, the extent of mangroves expanded significantly (p < 0.01, n = 14). Our results suggest mangrove expansion and tidal flat loss have considerably reduced shorebird habitat in 8 of these sites. To improve the overall conservation outcome, we devised a decision tree for addressing the dilemma. Important factors to consider include whether the area of interest is of importance to shorebirds and what the potential impacts of mangrove expansion are; what the value of the proposed mangrove ecosystem is compared with the existing ecosystem; and that a conflict‐resolution process will be needed if the choices are very similar. With careful consideration of alternative management strategies, decision makers can ensure that the conservation of mangroves does not imperil migratory shorebirds.


INTRODUCTION Current state and trajectory of mangrove habitat
Mangroves occur in the intertidal zone, where they are regularly inundated by seawater, and are most abundant and diverse in the tropics (Giri et al., 2011). Mangrove ecosystems provide important ecosystem services, including shoreline protection (Sun & Carson, 2020), water quality and climate regulation through carbon storage (Donato et al., 2011;Lovelock & Reef, 2020;Murdiyarso et al., 2015), pollutant uptake and nutrient cycling (UNEP, 2014), food and nursery grounds for commercially important fishes and invertebrates (Aburto-Oropeza et al., 2008;Ronnback, 1999), and nesting habitat for coastal birds. Value estimations of mangrove ecosystem services range from US$4217 to $6938 per km 2 annually (Himes-Cornell et al., 2018). Globally, mangrove extent has decreased markedly, but has slowly recovered since 2000 in some areas (FAO, 2007;Giri et al., 2015). Global mangrove extent declined 0.66−1% annually in the 1980s, 3−5 times higher than the rate of global forest loss. An estimated one third of natural mangrove extent was lost from 1950 to 2000 (Alongi, 2002;FAO, 2007) due to timber production and conversion to aquaculture ponds and farmlands (Alongi, 2002;Bryan-Brown et al., 2020;Murdiyarso et al., 2015). The rate of loss slowed to an average of 0.13% annually from 2000 to 2016 (Goldberg et al., 2020) due to natural recovery, active restoration (at sites where mangroves had previously occurred), and afforestation (at sites where mangroves had not previously occurred). However, recent estimates suggest that 69% of the mangrove area in Indo-Pacific islands (Lovelock et al., 2015) and half of mangrove coverage worldwide (Alongi, 2015) are still threatened by sea-level rise, sediment subsidence, and low sediment accretion rate, although there is considerable uncertainty in these estimates (Schuerch et al., 2018).
Although the boundaries between mangrove, saltmarsh, and open tidal flat ecosystems are highly dynamic and vary between years due to factors such as changes in sedimentation rate, salinity, and accessibility by propagules (Cavanaugh et al., 2019;Saintilan et al., 2014), analysis of satellite images combined with ground truthing indicates rapid expansion of mangroves in many places around the world. These increases are due to natural dynamics (when the rate of sediment accretion exceeds the combined rate of subsidence and sea-level rise [Lovelock et al., 2015;Schuerch et al., 2018]) and active restoration and afforestation (Jia et al., 2018). Near their latitudinal limits, mangroves have expanded into space originally occupied by saltmarsh, a phenomenon observed on at least 5 continents, including the east coast of Australia (Giri & Long, 2016;Saintilan et al., 2014). Natural expansion has also occurred in New Zealand and Hong Kong, but this is primarily expansion from the upper tidal flat toward the lower tidal flat (Chan et al., 2011;Stokes et al., 2010). In addition to natural expansion, mangroves in several countries, such as China, Bangladesh, Cuba, and Indonesia, have recently increased through active planting (Chen et al., 2009;FAO, 2007;Lee et al., 2019;Spalding et al., 1997). In China (Figure 1), the extent of mangroves increased by 20% (from 18,702 to 22,419 ha) from 2000 to 2015 following the introduction of policies to protect and plant mangroves to safeguard key ecosystem services, such as carbon sequestration and storage, shoreline protection, and food provision (Jia et al., 2018). Indeed, efforts to restore ecosystem services and enhance biodiversity in mangrove forests are increasing globally (Bayraktarov et al., 2020).

The challenge of conserving mangroves, tidal flats, and shorebirds
During the nonbreeding season, coastal shorebirds primarily forage at low tide when tidal flats are most exposed and rest during high tide when tidal flats are largely inundated (Choi, 2015;Choi et al., 2014;. Shorebirds usually forage on exposed tidal flats and they rarely use densely vegetated areas such as mangroves and saltmarsh, although a small number of shorebird species roost in mangroves (Choi et al., 2017;Zwarts, 1988).
Recent increases in mangrove distribution have led to a conservation dilemma in some areas where mangrove expansion has replaced saltmarsh and bare tidal habitats-in many cases, critical shorebird habitat (Figure 1 & Appendix S1; Huang et al., 2012;Straw & Saintilan, 2006;Zou et al., 2006). This dilemma is particularly pertinent along the East Asian-Australasian Flyway (EAAF), which encompasses 45.6% of the global mangrove extent (Giri et al., 2011) and has the highest proportion (23%, 46 species) of threatened migratory waterbirds (Kirby et al., 2008). As one of the prominent groups among waterbirds, many migratory shorebird populations along the coast of EAAF have declined substantially, and this is linked to extensive loss of tidal flats along their refueling sites (Piersma et al., 2016;Studds et al., 2017); 11 shorebird species are currently listed as threatened under International Union for the Conservation of Nature categories vulnerable, endangered, or critically endangered, and an additional 10 species are listed as near threatened (IUCN, 2021).
Many countries have regulations directed at mangrove conservation or restoration, and some also have regulations to protect shorebirds or their tidal flat habitats. There is often a lack of clear guidance on how to resolve the potential conflict caused by this competition between mangroves and the habitats used by declining shorebird populations. We considered a number of cases in which this conflict has emerged and conducted an empirical investigation along the coastline of southern China by way of a worked example, building on earlier work that mapped the extent of mangroves (Jia et al., 2018) and documented important shorebird sites (Jackson et al., 2021). We also devised a decision tree to assist managers in addressing this dilemma and ensuring that conservation of mangroves does not imperil migratory shorebirds.

Case studies
Through personal experiences and concerns raised by local conservation practitioners, we became aware of 5 examples across the EAAF in which mangroves have expanded into saltmarshes or tidal flats at internationally important shorebird sites: the Firth of Thames on the North Island of New Zealand; Hunter Valley in Eastern Australia; Leizhou Peninsula and Shenzhen Bay in southern China; and Guandu on Taiwan Island (Table 1). All but 1 of these locations (Guandu) is designated as a wetland of international importance under the Ramsar convention (Ramsar, 2017), and all but 1 (Leizhou Peninsula) is an important bird area (BirdLife International, 2020). Some of these sites provide habitat for highly threatened shorebird species, such as the black stilt (Himantopus novaezelandiae) (critically endangered), spoon-billed sandpiper (Calidris pygmaea) (critically endangered), and eastern curlew (Numenius madagascariensis) (endangered). All sites are protected to some extent and have had mangrove expansion in recent years through natural dispersal or artificial afforestation (Figure 2) (Jia et al., 2018;Reid, 2019). Shorebird population and distribution changes have occurred in Hunter Valley and Guandu (Appendix S5). At some sites, local managers and stakeholders have physically    2015) and Conklin et al. (2014), which report coastal sites of international importance for shorebird species (i.e., sites meet Ramsar Convention listing criterion 6, hosting >1% of the flyway population). We considered only shorebird sites in Zhejiang or farther south because only these overlap the distribution of mangroves. The coastline of all sites comprises a hardened seawall, which is generally straightforward to discern and interpret in images or image composites in Google Earth. We therefore used the his- To map change in mangrove extent, we followed methods described in Jia et al. (2018). We adopted an object-based classification approach to interpret mangrove forests from Landsat images and used eCognition Developer 9.2 to process the classification. We obtained homogeneous objects by segmenting images based on 3 parameters: scale, compactness, and shape (Jia et al., 2018). Then we processed the nearest neighbor classifier (NN classifier) to classify objects into specific categories (mangrove or nonmangrove). We postprocessed the classification output by manually correcting misclassified objects (89−94% overall accuracy [Jia et al., 2018]). The difference in mangrove extent in 2000 and 2015 for each of the important coastal shorebird sites was then calculated (square kilometers).
To estimate tidal flat change, we followed the methods of The areal extent of mangrove and tidal flat in 2000 and 2015 was compared using nonparametric paired 2-sample Wilcoxon test (because data were not normally distributed) in R 3.6.3 (R Core Team, 2020). We used p < 0.05 as the significance level.

Decision tree approach
To help inform local decision-making on how and when to implement management actions on mangroves, we designed a decision tree that provides step-by-step guidance (Figure 4). In the first step, decision makers examine the area of interest and determine its importance to shorebirds (Figure 4, Q1). Some shorebirds have multiple foraging and resting sites and might switch if their original site is degraded or lost, whereas others do not . This redundancy might lead to certain sites being considered nonessential for shorebird conservation (Dhanjal-Adams et al., 2017). To address this problem, one could determine the presence of threatened shorebird species with the IUCN Red List of Threated Species or occurrence records on shorebird distribution patterns. If the area is of low importance to shorebirds (abundances or species threat status does not meet Ramsar site criteria [Ramsar, 2017]), then there is not a strong trade-off between mangrove restora-tion and afforestation and shorebird conservation. The decision makers might move on to considering other factors involved, such as economic cost and carbon sequestration capacity, in the decision to manage mangroves.
In the second step, for sites that were identified in step one as being important to shorebirds, decision makers estimate the potential impacts of mangrove expansion (Figure 4, Q2). Remote sensing and field survey data may be used to quantify trends in mangrove and tidal flat extent (Jia et al., 2021;Swales et al., 2009), and plantation plans (spatial extent and quantity) by local stakeholders should also be considered (Choi et al., 2017;Sievers et al., 2020). For example, mangrove restoration through converting some aquaculture ponds back to mangroves is likely to have a lower impact on shorebird habitats than mangrove afforestation on open tidal flats where mangroves did not previously occur. It is also important to ensure that sufficient hightide roosting habitat (which can include aquaculture ponds; Jackson et al., 2020) is retained. Even where a low impact of mangrove expansion is expected, we suggest a conservative approach of monitoring before and during the implementation of afforestation (McDonald-Madden, Probert, et al., 2010).
In the third step, where mangrove expansion is likely to result in loss of important shorebird habitat, decision makers could estimate the value of mangrove ecosystems to objectively assess the shorebird-mangrove trade-off (Figure 4, Q3). Several tools are available to evaluate the value of an ecosystem, such as the System of Environmental Ecosystem Accounts (United Nations, 2021), which was published to create a set of ecosystem accounts (extent account, condition account, and ecosystem services account), in both physical and monetary values, to record the value of and changes in ecosystem and ecosystem services (Sanchirico et al., 2015;UN Sustainable Development, 2017). After the assessment, if the mangrove ecosystem value is considered lower than the original ecosystem value with shorebirds and other habitat features (e.g., tidal flat, saltmarsh), the implication is clear-managers would limit the further spread of mangroves. For example, if local policy sets very high values on endangered shorebirds, this might mean compulsory protection of particular species regardless of the ecological value of alternative policies (Lau & Shi, 2000). Besides, planting mangroves in the wrong place could have negative impacts on other components of the coastal ecosystem, such as saltmarsh and sea grass, because those vulnerable ecosystems could be trampled by planting volunteers or overgrown by mangroves, a problem that could worsen if non-native mangrove species are planted (Wetlands International, 2016).
If the decision is finely balanced, a conflict resolution process is entered into that seeks to investigate carefully the tradeoffs between planting mangroves for high-value service provision and preserving original habitats for endangered shorebirds and other habitat types (Xiao et al., 2018). In this case, more complex frameworks are needed, such as structured decisionmaking or working through a mitigation hierarchy as part of an environmental impact assessment (Jacob et al., 2016;McDonald-Madden, Baxter, et al., 2010). We used 1 of our 5 case studies-Shenzhen Bay-to illustrate implementation of the decision tree for conservation decision-making.

Mangrove and shorebird dilemma in China
Within the 22 important coastal shorebird sites we mapped in southern China, mangroves were present in 14 sites. At 11 sites mangrove extent increased, and in 3 mangrove extent decreased from 2000 to 2015. The areal extent of mangrove in 2015 (all sites combined total = 58 km 2 ) was significantly larger than that in 2000 (all sites combined total = 42.2 km 2 ) (Wilcoxon signed rank test, V = 8, p < 0.01, n = 14). Among the 11 sites with an increase in mangrove extent, expansion was 16 km 2 (max = 8.5 km 2 , min = 0.1 km 2 , n = 11), at a mean rate of 0.1 km 2 (SE = 0.05) per site per year (n = 11) and an overall mean change of 156.4% (SE = 67.7) (n = 8 with 3 other sites excluded in the calculation of mean because no mangroves occurred in 2000). In contrast, the areal extent of bare tidal flat in 2015 was significantly smaller than in 2000 (Wilcoxon signed rank test, V = 225, p < 0.01, n = 22). Among the 11 sites with mangrove expansion, the extent of bare tidal area declined in 9 sites (81.8%) (max = 23.7 km 2 , min = 0.13 km 2 , n = 9) at a mean rate of −0.43 km 2 (0.16) per year (n = 9) and an overall decrease of 18.3% (4.1) (n = 9) (Figure 3 & Appendix S4).

Decision tree application
Shenzhen Bay is located at the Pearl River Estuary in southeast China. The wetlands around the bay provide important winter-ing and stopover habitats for about 40,000 migratory shorebirds Sung et al., 2021), including 4 critically endangered or endangered and 9 near-threatened shorebird species (Figure 4, Q1-High). Mangroves have expanded in the bay for the last 3 decades, mainly through natural dispersal (Figure 2b). This could significantly affect shorebird populations, many of which are declining significantly Studds et al., 2017), by reducing the extent of their foraging areas. As a result, local managers and stakeholders have actively removed mangrove seedlings or cut the stumps of mangrove trees to slow down mangrove expansion and preserve open tidal flats for shorebird to forage (Agriculture Fisheries & Conservation Department, 2011) ( Figure 4, Q2-High). However, those efforts were not always supported by local policies due to the conflicting demands of mangroves and shorebirds (Agriculture Fisheries & Conservation Department, 2011), making it prudent to implement research (e.g., natural capital accounting) to assess the mangrove ecosystem values relative to shorebirds (Figure 4, Q3). Once this has been achieved, managers might return to the decision tree to decide whether avoidance of further mangrove spread is warranted.

DISCUSSION
Our results demonstrate the importance of taking a holistic view of coastal ecosystem management. Considering any particular component, such as mangroves or tidal flats, separately from the others could lead to unintended negative consequences for the FIGURE 4 Decision tree for determining management options to restore mangroves or conserve tidal flats for shorebirds whole system. Despite an overall global decline in their extent, mangroves have expanded in many areas of the world due to active restoration, afforestation, and natural dispersal. However, our results demonstrate that this expansion can lead to a dilemma between mangrove and shorebird management in conservation decision-making. This problem has especially come to the fore in regions where migratory shorebird populations are declining rapidly. Our decision tree can help guide decisionmaking in situations of potential conflict. It can be used to formulate optimal solutions and ensure that mangrove restoration or afforestation does not lead to negative impacts on other important ecosystem components, particularly the increasingly threatened shorebirds that depend on these coastal habitats. In many cases, a regional approach may be needed to ensure that effective mangrove conservation is achieved alongside meeting other coastal conservation goals.
Among the important shorebird sites with mangroves present in mainland China, a majority (79%) showed mangrove expansion from 2000 to 2015, suggesting that the dilemma between mangrove and shorebird conservation has become widespread in southern China. In mainland China, there are policies such as the Forest Law of the People's Republic of China and the Wetland Protection Law that provide guidelines on mangrove protection and management. China's unprecedented investment in sustainability has led to the implementation of a series of ecological projects to restore natural habitats (Bryan et al., 2018), such as the National Coastal Shelterbelt System Construction Project Plan (2016)(2017)(2018)(2019)(2020)(2021)(2022)(2023)(2024)(2025), which together with other similar projects has resulted in a marked increase in the areal extent of mangrove forest since 2000, mainly through afforestation and restoration (Jia et al., 2018;Paulson Institute, 2020). The latest mangrove conservation and restoration action plan aims to increase the current extent of mangrove forest by at least 30% by 2025 through active planting and substantial financial support to local departments (The Ministry of Natural Resources & the National Forestry & Grassland Administration, 2020; The State Council of the People's Republic of China, 2020). China has also seen a significant conservation effort directed toward migratory shorebirds and their habitats in recent years (Choi et al., 2022;Yang et al., 2020), for example, through the inscription of 3 tidal sites onto the World Heritage list in 2019 and another ∼14 sites to be considered for World Heritage Listing within the next 3 years, with nominations based in large part on the importance for threatened waterbirds (IUCN, 2019).
Such a rapid and positive change in attitude toward nature conservation is encouraging, but also poses a challenge to ecosystem managers (Fan et al., 2020)-in this case ensuring the costs and benefits of mangrove restoration or afforestation effort are fully evaluated so that potential negative impacts on shorebirds or other coastal conservation values can be carefully mitigated. Good decision-making will balance the relative benefits of mangrove expansion and tidal flat conservation by taking into account which areas are of highest importance to biodiversity, including shorebirds.